Zoomorphology
Zoomorphology (1987) 106:279-288
© Springer-Verlag 1987
Fine structure and presumed functions
of the pediceHariae of
Echinocardium cordatum (Echinodermata, Echinoida)
Marianne Ghyoot, Chantal De Ridder, and Michel Jangoux
Laboratoire de Biologie marine (CP 160), Université libre de Bruxelles, 50 ave F.D. Roosevelt, B-1050 Bruxelles, Belgium
Summary. Tridactylous, trifoliate, and globiferous pedicellariae occur on the body surface of Echinocardium cordatum. Tridactyles have three forms: the typical, the rostrate,
and the large forms. Both typical and rostrate tridactyles
and trifoliates occur all around the echinoid body (trifoliates are, however, 4 times more numerous than tridactyles). Large tridactylous and globiferous pedicellariae are
restricted to the peribuccal area.
As a general rule tridactyles and trifoliates are similar
in morphology. The distal part of the valves forms an open
blade and bears lateral teeth and/or denticles (single or in
combs). The stalk consists of a rigid proximal part supported by an axial rod and a fexible distal part which
includes an axial fluid-filled cavity. The cavity is surrounded
by muscle fibers and acts as an hydroskeleton, allowing
the undulating-coiling movements of the flexible part of
the stalk. Trifoliates are always active while tridactyles react
only to direct or indirect mechanical stimulation.
The valves of the globiferous pedicellariae have a tubular distal part whose upper opening is surrounded by teeth.
There is no differentiated venom gland but a cluster of
epithelial glandular cells located at the level of the valve
upper opening. A small citiary pad occurs just below the
glandular cluster. Globiferous stalks are not flexible, being
supported for their full length by an axial rod. Globiferous
pedicellariae appear to be sensitive only to chemical stimulation.
The presumed functions of E. cordatum pedicellariae
are (1) cleaning of the body surface and ciliary structures
(trifoliates), (2) protection against sedimenting particles (tridactyles), and (3) defense of the peribuccal area against
potential small predators (globiferous pedicellariae).
A. Introduetion
Echinoids harbor various types of pedicellariae (for review
see Campbell 1983) the fine structure of which have been
rather intensively studied in regular echinoids (e.g., Cobb
1968a, b; Campbell 1972; Oldfield 1975, 1976; Hilgers and
Splechtna 1976, 1982). Almost no authors except taxonomists (e.g., Döderlein 1906; Koehler 1927; Mortensen 1951)
describe the general morphology of the pedicellariae borne
by burrowing echinoids, namely spatangoid irregular echinOffprint requests to ." M. Ghyoot
oids. This paper deals with the pedicellarial cover of the
common European spatangoid Echinocardium cordatum
(Pennant, 1777). Its goals are to describe the structure and
consider the function of each type of pedicellaria in relation
to regular echinoids.
B. Materials and methods
E. cordatum was collected from the intertidal zone on a
sandy beach at the Le Home-Varaville, Normandy, France
(mean size of individuals: 55+ 5 mm in length, 52+ 5 m m
in width). They were maintained in aquaria (12 ° C) either
at the marine laboratory of Luc-sur-mer in Normandy
(open-circuit marine aquarium) or at the University of
Brussels (closed-circuit marine aquarium).
Estimation of pedicellarial densities was carried out
both on whole individuals and selected body-wall areas (ca.
5 x 5 mm) (Fig. 1). The latter were removed and observed
in vitro with a stereomicroscope. Densities of globiferous
and large tridactylous pedicellariae were estimated by
counts in the five ambulacral regions of the peribuccal area
(Fig. 2A). Pedicellarial movements were observed on individuals placed in heightened petri dishes without current,
using a stereomicroscope. Mechanical stimulation of the
pedicellariae was performed with dissecting needles.
For light microscopy, pedicellariae were fixed and decalcified in Bouin's fluid, embedded in paraplast and cut into
5 ~tm thick sections. Sections were stained according to the
procedure of Ganter and Jollès (1969, 1970). The routine
stains were: Groats' hematoxylin with phloxine and light
green; Masson trichrome; Alcian blue, pH 2.6, with previous permanganic-sulfuric oxidation. Histochemical observations were performed using the Alcian blue pH 2.6 method, the PAS method for the detection of mucopolysaccharides, and Danielli's method for the detection of proteins.
For scanning electron microscope (SEM) observations,
whole pedicellariae were fixed in Bouin's fluid (without
acetic acid), dehydrated in graded ethanol and dried by
the critical point method using CO2 as transition fuid. The
pedicellarial skeleton was prepared for the SEM by dissolving the soft tissues of 70% ethanol-preserved pedicellariae
with sodium hypochlorite. Detached ossicles were washed
in distilled water and stored in 70% ethanol. Both whole
pedicellariae and pedicellarial ossicles were mounted on aluminium stubs, coated with gold in a sputter coater and
observed with an ISI DS-130 scanning electron microscope.
280
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JII
I~
11
Fig. 1A-C. Localization of the selected body wall areas of Echinocardium cordatum (stippled areas, ca. 25mm 2 each) used for the
estimation of pedicellarial densities. Drawings represent the aboral (A), oral (B), and posterior (C) surfaces of an echinoid
Table I. Mean length (mm) of pedicellariae of Echinocardium cordatum (m _+s.d.) a
Type of pedicellaria
Length of the head Total length
of the pedicellariae
Length of the flexible part
of the stalk
Length of the rigid part
of the stalk
Globiferous
range
Trifoliate
range
Typical tridactylous
range
Large tridactylous
range
Rostrate tridactylous
range
0.7 __+0.05
0.6 - 0 . 8
0.1 ___0.02
0.12-0.16
0.5 _ 0.1
0.4 - 0 . 6
1.4 __+0.2
1.2 - 1.7
0.4 ___0.1
0.3 - 0 . 6
-
1.3+0.1
1.1 - 1.4
0.9+0.2
0.6-- 1.1
1.4 _ 0.2
1.2-1.7
1.5 _ 0.4
0.9 - 2.2
1.2 _+0.1
1.1-1.4
2 +0.15
1.7-2.1
2.3+0.3
1.7-2.7
4.2 _+1.4
2.7-6.2
4.1 + 0.8
2.8 - 5.3
2.3 + 0.3
2.1-2.8
1.3+0.2
1.0-- 1.5
2.3 __+t .2
1.0-4.3
1.2 +_0.5
0.7 - 2.0
0.7 + 0.2
0.4-0.9
a Measurements taken from 10 pedicellariae of the oral surface of one individual (test dimension: 50 mm length, 48 mm width)
C. Results
L General shape, distribution and density ofpedicellariae
Three types o f pedicellariae occur in E. cordatum, namely
tridactylous, trifoliate, and globiferous pedicellariae. Each
type basically consists of a three j a w head and a stalk,
the latter being attached to the echinoid body. Each j a w
is supported by an ossicle or valve. The stalk is either wholly
rigid, being supported t h r o u g h o u t b y a calcareous rod (globiferous pedicellariae), or partly flexible, the supporting rod
occurring only in the basal p a r t o f the stalk (trifoliates and
tridactyles). Moreover, there are three forms o f tridactylous
pedicellariae: a typical, a large, and a rostrate form. They
differ from each other by either the shape or the length
o f the jaws, and the length o f the flexible p a r t o f the stalk.
M e a n measurements of each pedicellarial type and form
are given in Table 1.
Trifoliates and typical and rostrate tridactyles occur everywhere on the echinoid b o d y surface. M e a n densities o f
these two pedicellarial types in selected b o d y areas are rep o r t e d in Table 2 (see also Fig. 1 A - C ) . Trifoliates and tridactyles each have a rather even density all a r o u n d the
echinoid body, trifoliates being, however, 4 times m o r e numerous than tridactyles. Both large tridactylous and globiferous pedicellariae were seen almost exclusively on the oral
surface near the m o u t h (Fig. 2A). As seen in Table 3, globi-
ferous pedicellariae are most dense in the posterior region
o f the peribuccal area while large tridactyles are more uniformly distributed. The latter, however, never occur on the
labrum (Fig. 2 B). It should also be noted that some individuals were totally devoid o f globiferous a n d / o r large tridactylous pedicellariae and were not considered when estimating pedicellarial density. Moreover, large tridactyles occasionally occurred on a m b u l a c r a I and V outside the peribuccal area, and there were rare instances o f a single globiferous pedicellaria a r o u n d the anus.
IL Structure of the pedicellariae
All pedicellariae consist o f intradermal ossicles one valve
per jaw and one r o d in the stalk - embedded in dermal
tissue. They are entirely covered by a cutaneous epithelium
that develops in places o f ciliary structures. S E M preparations o f whole pedicellarial heads show that the basal parts
o f the jaws are always found in a c o m m o n dermal sheath
while their apical parts are free. W h e n closed, the jaws are
in contact either distally (tridactylous and globiferous pedicellariae; Figs. 3, 4) or for their full length (trifoliates;
Fig. 5). The outer surfaces o f pedicellariae are almost perfectly smooth; teeth, denticules, and other skeletal p r o t u berances are either embedded in dermal tissue or covered
by an epidermal layer.
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Table 2. Mean densities of trifoliate and tridactylous pedicellariaea
Periproctal area
(Fig. 1 C)
Aboral surface (Fig. 1 A)
Oral surface (Fig. 1 B)
Peribuccal area Peristome Ambulacrum 1
Plastron
Ambulacrum 1 Interambulacrum 4/5
Trifoliate
meanvalue_+s.d.
range
20.3_+ 7.0
11 - 3 4
11.3_+ 5.0 28.4_+12.6
5 -20
10 - 5 2
19_+ 7.9
8-32
24.9_+ 7.0
16 - 3 8
Tridactylous b
meanvalue_s.d.
range
5.8_+ 2.9
3 -13
4.5_+ 3.1
1 -10
7.3_+ 5.0 3.1___1.1
2 -16
1 -5
5.7_+ 4.7
1 -16
28.7_+ 10.4
17 - 4 5
27.3_+ 7.8
21 - 4 8
3.0 _ 1.3
2 -5
6.8___ 5.7
2 -20
" mean number of pedicellariae per 25 mm 2 (n = 10 echinoids, p = 0.05) (see Fig. 1 A~S)
b typical and rostrate forms were not segregated; large forms were not considered (see Table 3)
in-
I
]JE
~/-
I
Fig. 2A, B. Distribution of globiferous and large
tridactylous pedicellariae in the peribuccal area of
Echinocardium cordatum. A Subdivisions of the
peribuccal area used for the counting of
pedieellariae. B Globiferous and large tridactyles
occur together in the dense stippled region; large
tridactyles are never seen in the spaced stippled
region where only globiferous pedicellariae occur
~-
Table 3. Mean number of globiferous and large tridactylous pedicellariae in the peribuccal area (n = 10 echinoids, p = 0.05)
Ambulacrum 1
Anterior
region
Lateral regions
Posterior region
Whole
peribuccal
area
Ambulacrum 5
Whole
region
Ambulacrum 4
Ambulacrum 2
Whole
region
Ambulacrum 3
Large tridactylous
meanvalue+s.d. 1 . 0 _ + 0 . 8
range
0 -2
1.9+1.7
0 -5
2.9_+2.1
1 -7
1.4+1.3
0 -4
1.2-t-1.8
0 -6
2.6_+3.0
0 -10
0.5_+0.5
0 -1
6.7___ 5.4
1 -16
Globiferous
meanvalue_+s.d. 2.9_+2.9
range
0 -9
2.4+__1.9
0 -6
5.3_+ 4.6
1 -15
0.9+1.8
0 -6
0
0
0.9+1.8
0 -6
0.5___0.8
0 -2
6.0_+ 4.8
1 -17
1. Tridactylous pedicellariae. Tridactylous valves have a lancet-like shape. They consist o f a basal, a proximal, and
a distal p a r t (Figs. 6, 9). The distal p a r t is narrow, relatively
pointed, a n d spout shaped. It bears a single median distal
t o o t h and numerous lateral minute denticules. The proximal p a r t is enlarged, being triangular to r h o m b o i d a l in
shape, a n d deepens into two large cavities separated by
a median wall. The basal part consists o f a posterior bulge,
a relatively flat median area, and an anterior series o f parallel cristae (Fig. 9).
M e a n measurements o f tridactyle jaws are given in Tabie 1. Jaws o f typical and rostrate forms are rather similar
in length while those o f large tridactyles are a b o u t 3 times
longer (Figs. 6 to 8). In typical tridactyles the distal p a r t
o f the valve is slightly longer than the p r o x i m a l part. Rostrate valves are m o r e dumpy, their distal p a r t being shorter
than their proximal part. The distal p a r t o f the large tridactyle valve is considerably longer, usually 3 times as long
as the proximal part. Opening a n d closing o f the jaws are
due to the action o f three bundles o f a b d u c t o r and a d d u c t o r
muscles. A d d u c t o r muscles are conspicuously developed;
they consist o f smooth a n d striated fibers, the latter forming
the lower p a r t o f each bundle (Fig. 11). A d d u c t o r s attach
within the twin cavities o f the p r o x i m a l part o f the valve
(Figs. 6 to 9), each bundle running from one cavity to the
nearest cavity o f the adjoining valve. A b d u c t o r muscles are
282
Figs. 3-5. Scanning electron micrographs of the heads of Echinocardium cordatum pedicellariae. Fig. 3. Tridactylous pedicellaria (typical
form). Fig. 4. Globiferous pedicellaria. Fig. 5. Trifoliate pedicellaria
less developed. They consist only o f smooth fibers that attach to the base of the bulge (Fig. 9) and are arranged
parallel to the adductor bundles.
The tridactyle stalk is flexible distally but rigid proximally due to an axial supporting rod (Figs. 10, 12). The
rod is slightly enlarged apically and articulates on a small
test tubercle consisting o f a peripheral areole, a median
boss (slope area), and a small central mamelon (Fig. 13).
The rod develops a slight basal widening (trabecular outgrowths; Fig. 10) that corresponds to the attachment area
of the stalk flexor muscle which runs down to the areole
of the tubercle. The distal part o f the stalk has no rod
but does have a rather narrow and fluid-filled axial cavity
(Fig. 11). The axial fluid includes mucosubstances as it
reacts positively to both the PAS and Alcian blue methods.
The dermal tissue surrounding the cavity is crossed by fibers
of the head flexor muscles. These muscles run from the
bulge o f each valve down to the distal extremity of the
rod, some fibers anchoring also within the dermal tissue
close to the cavity. Head flexor muscles allow the bending
movements of the head over the stalk and the undulating/
coiling movements of the flexible part o f the stalk. The
latter are due to fibers that anchor near the axial cavity
which acts as an hydrolic skeleton.
The outer epithelium of a tridactyle is rather smooth.
However, ciliary structures occur both along the stalk,
where two longitudinal and opposite rows of cilia are seen
(Figs. 14, 15) and on the jaws, the inner sides of which
are lined with cilia.
2. Trifoliate pedicellariae. Trifoliates valves are very small
(Table 1). Their proximal and basal parts are similar to
the corresponding parts o f tridactyles (Fig. 16) while their
distal parts are rather different, being broad, blunt-tipped,
and more or less spoon-shaped. Valves are fringed apically
by a series o f small denticles (Fig. 17). Their sides bear
protruding combs of distal denticules (Figs. 5, 18) and a
proximal series of single teeth. Proximal teeth are embedded
in the dermal tissue; they are imbricate when the valves
close (Figs. 17, 18). Except for their size and valve architecture, trifoliates look like tridactyles. Abductor and adductor
muscles are similarly arranged to those of tridactyles but
consist only of smooth fibers. The stalk is also similar and
includes a distal fluid-filled cavity (Fig. 19) and a proximal
rod which is, however, much more slender (Fig. 20).
3. Globiferous pedicellariae. Globiferous valves have a glo-
bulous appearance (Fig. 4) due mainly to the thinness of
the distal part, which forms a hollow tube whose upper
opening is surrounded by a series of teeth (Figs. 21, 22).
Figs. 6-15. Tridactylous pedicellariae of Echinocardium cordatum. Fig. 6. Inner view of the valve of a typical tridactyle. Fig. 7. Inner
view of the valve of a large tridactyle. Fig. 8. Inner view of the valve of a rostrate tridactyle. Fig. 9. Profile view of the basal part
of a valve. Fig. 10. Side view of the stalk supporting rod. Fig. 11. Longitudinal section through a jaw and the upper part of the
flexible stalk (the inset illustrates the occurrence of striated adductor fiber). Fig. 12. Scanning electron micrograph preparation of a
whole pedicellaria. Fig. 13. Tubercle of articulation. Fig. 14. Longitudinal ciliary tract of a stalk. Fig. 15. Enlarged view of a stalk
ciliary tract, a areole; ab abductor muscle; ac axial cavity; ad adductor muscle; b basal part of the valve, bo median boss; bu bulge;
c cristae; ca cavity of the proximal part; ct ciliary tract; d distal part of the valve; f flexible stalk; h pedicellarial head; m mamelon;
p proximal part of the valve; r rigid stalk; t terminal tooth; w median wall
1 ~i~¸
284
Figs. 16-20. Trifoliate pedicellariae of
Echinocardium cordatum. Fig. 16. Inner view of a valve. Fig. 17. Profile view of a closed head
showing the lateral combs of denticles and the two series of imbricated lateral teeth. Fig. 18. Enlarged view of the lateral combs
of denticles. Fig. 19. Longitudinal section through the head and the upper part of the flexible stalk. Fig. 20. Enlarged view of the
basal part of the stalk supporting rod and of its corresponding test tubercle, a areole; ac axial cavity; ad adductor muscle; b basal
part of the valve; bo median boss; br basal part of the tod; c comb of denticles; ca cavity of the valve proximal part; d distal
part of the valve; da denticular apex; h head flexor muscle; j jaw; m mamelon; p proximal part of the valve; t lateral tooth; w
median wall
As a general rule, the proximal and basal parts o f the valves
are similar to those o f other pedicellarial types, although
the posterior bulge is less developed (Fig. 23). A b d u c t o r
and a d d u c t o r muscles are arranged similarly to the other
types. The a d d u c t o r muscles consist only o f smooth fibers.
The globiferous stalk is completely rigid, being supported by a strong and rather massive rod. The distal part
o f the rod is smooth and relatively short (Fig. 21). It attaches to the pedicellarial head through connective strands
which anchor to the cristae o f the basal part o f the valves
285
Figs. 21-28. Globiferous pedicellariae of Echinocardium cordatum. Fig. 21. Skeletal organization of a whole pediceUaria. Fig. 22. Inner
view of a valve. Fig. 23. Skeletal organization of the pedicellarial head (basal view). Fig. 24. Longitudinal section through a whole
pedicellaria. Fig. 25. Longitudinal section through the distal part of a jaw. Fig. 26. Cross section through the apical area of a jaw.
Fig. 27. Enlarged view of the basal part of the stalk supporting rod and of its corresponding test tubercle. Fig. 28. Longitudinal section
through the stalk/tubercle articulation area. a areole; ad adductor muscle; b basal part of the valve; bo median boss; br basal part
of the rod; bu bulge; c cristae; ca cavity of the valve proximal part; co connective strands; cp ciliary pad; d distal part of the valve;
dr distal part of the rod; h head flexor muscle; g glandular area; rn mamelon; n nerve tract; p proximal part of the rod; r rod;
s stalk flexor muscle; st stalk; t terminal tooth; tr trabecular outgrowths; w median wall
286
(Figs. 23, 24). The median part of the rod is the longest
(Fig. 21). It has a spiny appearance due to the development
of trabecular outgrowths that develop from the lower part
of the rod (Figs. 21, 27). These outgrowths - which presumably consolidate the stalk - run upwards, parallel to the
long axis of the rod. The proximal part of the rod is the
shortest (Fig. 21). It articulates on a test tubercle similar
to but larger than those of other pedicellarial types
(Fig. 27). Head flexor muscles run from the valve bulge
down to the distal part of the rod (Figs. 21, 24), while the
stalk flexor muscle runs from the proximal part of the rod
to the areole of the corresponding test tubercle (Figs. 24,
28).
The outer epithelium of globiferous is relatively smooth.
Scattered cilia occur, however, on the inner surface of each
jaw and a small ciliary pad is seen at the upper end of
the distal part of the jaw (Figs. 25, 26). A conspicuous nerve
bundle is associated with each ciliary pad (Fig. 25). Globiferous pedicellariae of E. cordatum do not have venom sacs
but rather an epidermal gland whose component cells have
granules containing acid mucosubstances and proteins. The
epidermal gland is just above the ciliary pad of the jaws,
at the level of the upper opening of the valve distal tube
(Fig. 25).
III. In vivo observations
In the absence of stimulation, tridactylous and globiferous
pedicellariae generally do not move. Typical and rostrate
tridactyles are usually erect, with their jaws either closed
or open. Large tridactyles hang from the oral body surface
with closed jaws. The globiferous pedicellariae are quite
variable, being either erect or resting on the body surface,
with open or closed jaws. Trifoliates are always intensively
active; they have a highly motile stalk that moves unceasingly in every direction in an undulating coiling movement.
Their jaws were often seen to open and close continuously,
either scraping the echinoid body surface or rubbing against
neighboring spines or pedicellariae.
Tridactyles show a searching reaction when the outer
surface of the jaws or the stalk or the surrounding body
structures (i.e., body surface and neighboring appendages)
are mechanically stimulated. Such reactions, however, are
almost never directed towards the stimulation source. More
specific reactions occur when the inner surface of the jaws
is mechanically stimulated. There is a rapid and strong closure of the jaws, which open again a few seconds later.
The globiferous pedicellariae almost never react to mechanical stimulation, yet do to chemical stimulation. Detached
tube feet of the asteroid Asterias rubens placed close to
them sometimes induced a conspicuous opening and closure
of the jaws followed by the autotomy of the whole pedicellaria.
D. Discussion
While pedicellariae commonly occur in all described species
of spatangoids (see Döderlein 1906; Mortensen 1951), investigations on their structure and functions are almost non
existent. Spatangoids harbor similar pedicellariae to regular
echinoids although they have a clearly different mode of
life, being buried rather deep in the sediment. Actually E.
cordatum possesses all the pedicellarial types classically described for regular echinoids, i.e. tridactylous, trifoliate, and
globiferous pedicellariae (see Campbell 1983), with the exception of ophiocephalous ones.
The high polymorphism of E. cordatum tridactyles is
noteworthy. Two of the three forms, the typical and rostrate, are uniformly distributed around the echinoid body
while large tridactyles are seen almost exclusively in the
peribuccal area (see also Koehler 1927). The restriction of
large tridactyles and globiferous to particular body areas
is in contrast to regular echinoids, which have rather uniformly distributed pedicellariae. Variations in density may,
however, occur (e.g., Mendes 1965; Ramsay and Campbell
1985). Moreover, globiferous and large tridactylous pedicellariae are not always present and individual E. cordatum
may lack one of these types or both.
The pedicellariae of E. cordatum may be grouped into
two categories according to the structure and relative motility of the stalk. Rigid stalks are seen only in globiferous
pedicellariae, as in most regular echinoids (Cannone 1970;
Chia 1970; Campbell 1973; Oldfield 1976). Tridactyles and
trifoliates are much more motile as the distal part of the
stalk has no supporting rod but rather a fluid-filled axial
cavity which acts as a hydroskeleton (Chia 1969). Flexible
stalks have been found in most tridactylous, trifoliate, and
ophiocephalous pedicellariae (e.g., Uexküll 1899; Chia
1969; Hilgers and Splechtna 1976; Splechtna and Hilgers
1980). The fluid of the axial cavity of E. cordatum pedicellariae contains mucosubstances; Chia (1969) also found
them in the axial cavity of the pedicellariae of the clypeasteroid Dendraster excentricus. Hilgers and Splechtna (1976)
reported that flexible stalk movements are produced by the
interplay of flexor muscles and connective strands. It should
be emphasized that no peristalsis occurs along the stalk
axial cavity as the surrounding flexor muscles consist only
of longitudinal fibers. The rather complex movements of
flexible stalks undoubtely results from the particular arrangement of the flexor muscles, some fibers of which anchor in the dermal tissue around the axial cavity. This anchoring and the independent contractions of individual
fibers allow the observed undulating and coiling movements.
Particular ciliary tracts are seen all along the stalk of
both tridactyles and trifoliates but do not occur on globiferous stalks. Such tracts also occur along the shaft of most
spines. They are presumably involved in the production
of superficial water currents that both allow the oxygenation of individuals and prevent the sedimentation of fine
particles on the body surface.
E. cordatum tridactyles strongly resemble those of regular echinoids in ossicle shape, ciliary structures, and occurrence of striated adductors (Cobb 1968a, b; Campbell
1972). According to Campbell and Rainbow (1977), their
function is to pick up less active or inert objects from the
body surface and possibly to capture small swimming organisms. E. cordatum tridactyles obviously have a powerful
grasp; they also clearly react to mechanical stimulation,
producing both the erection of the stalk and the undulatory/
coiling movements of the flexible section. This searching
reaction, however, is almost never directed towards the
stimulation source. Moreover, we never saw them picking
up particles that settled on the echinoid body or selectively
catching small organisms swimming around them. Closure
of tridactyles occurred mostly when the inner side of the
jaw was stimulated. Given that the stalk reacts to stimulation in a non-directed way, stimulation here and thus cap-
287
ture of particles or of swimming organisms may occur only
by chance. Such behavior is similar to that of pedicellariae
of the asteroid Marthasterias glacialis (see Lambert et al.
1984). Lambert et al. reported that M. glacialis pedicellariae
clearly react to mechanical stimulation but at random and
they lack coordination. They interpretated this behavior
as a protective activity which, taken as a whole, prevents
unwanted material and organisms gaining access to the asteroid body surface. Similarly E. cordatum tridactyles may
function to, e.g., prevent access to the body surface of sediment particles which could fall down accidentally from the
burrow wall.
E. cordatum tridactyles are highly polymorphic. This
does not result from remodelling of the valves but only
of the relative proportions of their proximal and distal
parts. From the three co-occurring forms of tridactyles only
two, the typical and rostrate forms, are distributed all over
the echinoid body. Typical and rostrate tridactyles differ
in their total length, rostrates being 2 times smaller than
typical tridactyles. This implies that there are two levels
of protection above the echinoid body surface, the most
superficial one being that of typical tridactyles. The dumpier and slightly shorter jaws of the rostrate form might
result from their location, close to the body surface. The
space between the spine bases is reduced and consequently
tridactyles would need shorter jaws to be efficient. Large
tridactyles occur almost exclusively in the peribuccal area.
Their location is presumably linked to the low density of
spines around the mouth, a situation that both entails the
development of larger protective appendages and allows
the action of enlarged jaws. The activity of large tridactyles
in the echinoid peribuccal area is also probably facilitated
by gravity, as the force developed by the flexible stalk alone
may be insufficient to lift such enlarged and weightened
jaws.
The fine structure of trifoliates has only been investigated casually (Campbell 1972). They show basically the
same architecture as tridactyles except in the distal part
of the valve. Trifoliates of regular echinoids scrape the body
surface (Campbell and Rainbow 1977). They are constantly
active (stalk movements), with jaws which can open independently of each other (Campbell and Laverack 1968).
A similar behaviour occurs in E. cordatum trifoliates which
very often contact either the body surface or neighbouring
appendages, i.e., spine shafts and pedicellarial stalks. Due
to their very small size it is quite difficult to see how they
work, except to note that each jaw opens and closes regularly. Basic movements of the head are either to scrape
the body surface or to rub against the neighboring appendages. Such movements suggest that the function of trifoliates might be both to resuspend small particles from the
body surface and clean the ciliary tracts of neighboring
appendages by using the apical and lateral denticles of their
jaws. This would allow an optimal ciliary activity in cleaning away unwanted particles that are then eliminated by
the ciliary currents.
Globiferous pedicellariae of E. cordatum have more differences than similarities to those of regular echinoids although both have the same globulous aspect and a rather
similar skeletal architecture. Globiferous jaws from regular
echinoids have three basic characteristics, namely (1) a conspicuous venom gland located between the outer epiderm
of the jaw and the outer side of its valve (Chia 1970; Cannone 1970; Holland and Holland 1975), (2) a well-devel-
oped venom tooth borne by the apical extremity of the
valve (Chia 1970; Cannone 1970; Campbell 1972; Oldfield
1976), and (3) an elaborated sensory equipment consisting
of an apical sensory pad and a basal sensory hillock both
located on the inner surface of the jaws (Cannone 1970;
Oldfield 1975). Globiferous jaws of E. cordatum do not
harbor a typical venom gland but develop small clusters
of epidermal glandular cells at the upper end of their inner
surface. These cells secrete a mixture of acid mucosubstances and proteins, yet it is not known whether these
are poisonous. Along with the absence of venom glands,
there is no venom tooth and each valve ends in a hollow
tube whose distal aperture is surrounded by a few small
teeth. The sensory equipment of E. cordatum globiferous
pedicellariae is also reduced and consists only of small sensory ciliated pads just below the cluster of glandular cells.
According to Campbell and Rainbow (1977) in regular
echinoids globiferous pedicellariae repel large animals such
as predators. E. cordatum globiferous pedicellariae, however, do not develop the conspicuous reaction described
by Jensen (1966), Campbell (1976), and Hilgers and
Splechtna (1982) for regular echinoids. They hardly react
to mechanical stimulation, but are still relatively sensitive
to chemical stimulation (i.e., stimulation by isolated tube
feet of asteroids). That globiferous pedicellariae of E. cordaturn are defensive appendages seems obvious considering
their overall morphology, behavior, and specialized location (around the mouth in an area partly deprived of spines
where important feeding appendages occur). Yet it is difficult to assess whether or not they are efficient defensive
appendages considering the weak development of both their
sensory equipment and their presumed poisonous structures.
In conclusion E. cordatum has a well-developed pedicellarial cover which acts at three different functional levels,
namely (1) the cleaning of the body surface and ciliary tracts
(trifoliates), (2) the protection of the body surface from
sedimenting particles (tridactyles), and (3) the defense of
the individual against potential small predators (globiferous
pedicellariae). Given the high density and uniform distribution of trifoliates and typical and rostrate tridactyles, one
may assume that both cleaning and protection are efficiently carried out. However, scattered defensive pedicellariae occurs only in the peribuccal area. Moreover, both globiferous and large tridactylous pedicellariae (the latter being
also located around the mouth) may be totally absent in
some individuals. All this is presumably linked to the particular mode of life of E. cordatum: to be deeply buried into
the sediment is undoubtedly one of the most efficient protections against large predators.
Acknowledgernents. We thank J. Harray and M. Klinkert for technical assistance and Dr P. Le Gall for providing facilities at the
marine Laboratory of Luc-sur-mer. Research was supported by
an IRSIA grant to M. Ghyoot, and by FRFC grant no. 2.4506.83
from the National Fund for Scientific Research.
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Received June 29, 1986